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Using Operant Conditioning

and Desensitization to Facilitate


Vet e r i n a r y C a re w i t h C a p t i v e
Reptiles
Heidi Hellmuth, BSa,*, Lauren Augustine, BAa,
Barbara Watkins, MAa, Katharine Hope, DVMb

KEYWORDS
 Reptile  Training  Operant conditioning  Desensitization

KEY POINTS
 In addition to being a large component of most zoological collections, reptile species are
also becoming more and more popular as family pets.
 Reptiles have the cognitive ability to be trained in order to facilitate daily husbandry and
veterinary care. Desensitization and operant conditioning can alleviate some of the behav-
ioral and physiological challenges of treating these species.
 A survey of reptile training programs at zoos in the United States and worldwide reveals
that there are many successful training programs being used in zoological settings to facil-
itate veterinary care and minimize stress to the animal.
 Many of the techniques being used to train reptiles in zoological settings are transferable to
the exotic pet clinician. These techniques are useful for improving veterinary care in private
herpetological collections and for the family pet.

INTRODUCTION

Many reptile species have become increasingly popular as pets. Exotic animal veter-
inarians are well aware of the impact that stress can have on their patients, and how
that stress can impact both the quality of the examination and overall health of the
animal. Utilizing operant conditioning techniques during veterinary procedures can
decrease the stress associated with the visit and increase the effectiveness of the
procedures. This article examines how different training and conditioning techniques

The authors have nothing to disclose.


a
Department of Animal Programs, Smithsonian’s National Zoological Park, 3001 Connecticut
Ave, NW, Washington, DC 20008, USA; b Department of Animal Health, Smithsonian’s National
Zoological Park, 3001 Connecticut Ave, NW, Washington, DC 20008, USA
* Corresponding author.
E-mail address: hhellmuth@verizon.net

Vet Clin Exot Anim 15 (2012) 425–443


http://dx.doi.org/10.1016/j.cvex.2012.06.003 vetexotic.theclinics.com
1094-9194/12/$ – see front matter Published by Elsevier Inc.
426 Hellmuth et al

can facilitate improved veterinary care and management of reptiles in the home, at the
exotic animal clinic, and in zoological settings.

REPTILE HEALTH—DISEASES, DIAGNOSTICS, AND THERAPIES


Common Diseases Seen in Reptiles
Captive reptiles can develop a variety of illnesses, ranging from infectious to neoplastic
to husbandry-related. As with any species, a complete history and physical examina-
tion, with appropriate diagnostic testing, are essential to accurately diagnosing and
treating the animal. A challenge with many exotic species is to understand and mini-
mize stressors that can affect behaviors and physiologic parameters in order to obtain
the most accurate diagnosis. This section will review common diseases of reptiles,
examination and diagnostic testing, and how the stress during veterinary procedures
can affect interpretation and treatment of animal illnesses.
The exotic practitioner very commonly encounters husbandry-related illnesses in
reptiles, many of which are related to the precise environmental parameters (eg, temper-
ature, humidity, ultraviolet exposure, substrate) and diet that these species require.
Common husbandry-related problems seen in reptiles include dysecdysis, metabolic
bone disease, obesity, vitamin deficiencies, traumatic abscesses, and stomatitis. A thor-
ough examination of any reptile must require a complete investigation of its housing and
diet, both current and historical, to detect or rule out husbandry-related disease.
Infectious diseases are also frequently encountered in captive reptile species, both in
pets and in zoological collections. Of the infectious diseases, endo- and ectoparasite
infections can be simplest to diagnose, requiring a positive identification from a fecal
sample or skin sample, though other parasitic infections can necessitate more extensive
testing (eg, radiographs or gastric biopsy). Bacterial, viral, or fungal infections can be
slightly more challenging to diagnose; and usually require more extensive testing,
including oral, nasal, or cloacal swabbing for polymerase chain reaction or culture, blood
collection for culture, or serologies for identification of the etiologic agent.1
Finally, in addition to the reptile-specific husbandry and pathogen-related diseases,
captive reptiles experience degenerative, metabolic, traumatic, or neoplastic diseases
just as do nonreptile species. A thorough diagnostic examination must investigate all
likely causes of disease.

Effects of Stress in Evaluating Animal Health


Reptiles can react to psychological or physical stress in ways that make it difficult to
interpret behavior, examination findings, or laboratory values. Creating a less stressful
environment is important for observing natural behaviors such as ambulation, head and
eye movements, and response to stimuli. Stressed reptiles may display false symp-
toms of illness such as erratic behavior or feigning death, particularly seen in hognose
snakes (Heterodon spp), and increased respiration rates have been seen in response to
elevated corticosterone levels in western fence lizards (Sceloporus occidentalis).2
The physiological and physical stress that may occur during an examination can affect
diagnostic results and potentially harm the animal. Studies have shown that exogenous
administration of corticosteroids can cause hyperglycemia in certain lizard and snake
species.3–5 Decreased cholesterol content of liver, increased urea content of liver and
kidney, and increased activity of glucose-6-phosphatase in the liver and kidney has
been noted in lizards following corticosteroid administration.4 However, the response
to exogenous corticosteroids, and the production of endogenous steroids, can be
seasonal for some species.6,7 Exhaustive activity in laboratory crocodilians resulted in
a significant decrease in blood pH and a significant increase in blood lactate levels,8,9
Operant Conditioning Techniques with Reptiles 427

suggesting that forceful restraint in an examination may alter blood chemistry. Interest-
ingly, a study in painted turtles showed that when put in situations of forced anoxia,
glucose and lactate levels rose; however, during recovery corticosterone levels rose
as lactate fell, suggesting that steroids may play a role in lactate metabolism and clear-
ance.9 Additionally, handling alone can cause increased corticosterone levels which in
turn can cause increased energy demands in already compromised patients.10,11 Force-
ful restraint can lead to trauma (eg, fractures in an animal with metabolic bone disease or
osteomyelitis) and some herpetofauna will drop their tails in response to stressful
handling. Due to the physiologic and physical responses to stress, desensitizing captive
reptiles to handling can be important in developing an ability to perform a successful
examination, obtaining accurate diagnostics, and preventing injury to the animals.

The Reptile Examination


To minimize stress during the examination, the room or enclosure should be an appro-
priate temperature for the species in order to observe the animal’s behaviors as
normally as possible. External stimuli should be minimized, and if possible, species-
specific items may be used to help the animal feel more comfortable (eg, chameleons
may prefer to have a branch to hold on to during the examination).
The most important diagnostics in any reptile examination are a thorough history and
a complete physical examination. History must include information on husbandry
(substrate, lighting, humidity, temperature gradient), diet, exposure to other animals,
where and when it was obtained by the owner, behavior, appetite, fecal and urate produc-
tion, weight, and any other pertinent information related to the cause of the veterinary visit.
Prior to handling the animal, practitioners should attempt to observe its activity, appropri-
ateness, and ambulation. Latex gloves must be worn during the physical examination, and
experienced handlers should be employed to ensure the animal is comfortable and thus
maximize the diagnostic value of the exam. Most pet reptiles can be examined under
manual restraint alone. However, some species or individuals may require additional
restraint devices (such as tubes, poles, boxes, or protective gloves) or techniques (such
as placing visual barriers or employing the vasovagal response) in order to minimize move-
ment during the examination. Procedures usually performed in awake reptiles include
blood samples for hematology, blood chemistry, and blood culture; fecal samples; oral,
nasal, or cloacal swabs; aspirates; radiographs; and ultrasound. Diagnostics that require
anesthesia include rigid or flexible endoscopy, advanced diagnostic imaging, and surgery.

Therapies and Monitoring


It is important to ensure that thorough records, including regular weight, feeding, and
husbandry information, are maintained. The owner or keeper must be able to assess
the animal’s behavior, condition, and any physical abnormalities to note any changes.
Correcting husbandry concerns is a top priority for treating both husbandry- and non–
husbandry-related illness in reptiles. Sick reptiles should be kept at the high end of
their temperature gradient in order to increase their metabolic rate and support the
immune system. Humidity must also be carefully controlled depending on the
disease—for example, high humidity may benefit animals undergoing dysecdysis,
but may predispose an already compromised animal to secondary fungal infections.
Diet adjustments may need to be made including offering different types of prey, or
sometimes syringe or tube feeding or placing an esophageal feeding tube.
Systemic medications can be administered enterally or parenterally. Generally,
orally administered medications are most desirable as owners can administer them
at home, but oral drugs can be difficult to administer reliably in an effective time frame
depending on the animal’s feeding schedule and willingness to accept food and/or
428 Hellmuth et al

medication. Injectable medications are frequently administered subcutaneously, intra-


muscularly, intravenously, or intracoelomically, and are usually uncomplicated in
reptiles but do require increased veterinary attention to administer. Topical medica-
tions such as liquids, creams, or baths are also common therapeutics employed.
Most aspects of veterinary care, from diagnosis to treatment, can be facilitated with
operant conditioning. Additionally, trainers, who are well-versed in observing animal
behavior, are able to spot tiny changes in an animal’s behavior,12 which can be critical
to detecting subtle signs that may indicate a veterinary problem. This article will review
how training techniques can minimize stress and maximize veterinary care in captive
reptiles.

REPTILE COMMUNICATION AND COGNITION


Reptile Communication Channels
Communication is defined as “the cooperative transfer of information from a signaler
to a receiver.”13 Humans have very familiar ways of transferring information, inten-
tions, and desires with other mammals. Verbal cues and hand gestures are used
with great success when training other mammals that have acute vision and hearing.
However, reptiles have modes of communication that are less familiar and require
a different training approach. When training reptiles it is important to understand the
specific species’ communication channels. Generally speaking, communication in
reptiles occurs visually, acoustically, tactilely, and chemically, with animals often
relying on multiple methods to receive input simultaneously.13
Visual communication in reptiles can range from the movement of a specific body
part to dramatic color displays. An obvious example of visual communication is
a head bobbing display for courtship or territoriality in many species of lizard.13
Body coloration and color change can be sexually dichromatic and are forms of visual
communication.14 In laboratory studies conducted on highly visual lizard species,
females painted with male coloration elicited aggressive behavior from other males
when placed in terraria, and similar responses were documented when males were
painted with female coloration.14 Specific snake species, such as king cobras (Ophio-
phagus hannah), are highly visual hunters that respond to prey movement. It has been
suggested that tortoises seek out brightly colored vegetation in foraging for food15 and
crocodilians are known to be very visual predators.16 Many species utilize courtship
gestures, submissive postures, tail displays, and various signaling mechanisms in
communication.14
Auditory communication is evident with various reptile species across many taxa,
including vocal calls, bellowing, body parts being rubbed to produce a sound, and
slapping the body against a specific surface, such as head slaps in water with croco-
dilians.13 New research also indicates that snakes may in fact hear air-borne sounds.17
There is even evidence that a nonvocal reptile, the Galápagos marine iguana (Amblyr-
hynchus cristatus) can hear and utilize the alarm call of the Galápagos mockingbird
(Nesomimus parvulus) to respond with its own anti-hunter behaviors to their shared
predator, the Galápagos hawk (Buteo galapagoensis).18
In tactile communication, an animal uses its body to rub, press, or hit another
animal. In tortoises this manifests as neck biting, hindlimb stroking, chin rubbing,
spur stroking, shell ramming, and biting14; caudocephalic and cephalocaudal waves
are seen in snake courtship and are best described as contractions of movement
against the female’s body prior to copulation.14 Snakes interpret ground-borne
sounds through vibration transferred through the body to the skull,19 in addition to
air-borne sounds.17 This concept of sensation through touch can be used in a training
Operant Conditioning Techniques with Reptiles 429

program. For example, tortoises will respond to neck rubs and tactile reinforcers and
snakes can respond to cues that cause slight vibrations when training.
A primary mode of communication for many species of reptile is chemical signaling.
Many species rely heavily on skin and cloacal secretions during mating. An experiment
involving garter snakes (Thamnophis sirtalis and T butleri), where estrous females were
covered with petroleum jelly to conceal signaling by skin secretions, showed that
males that were once receptive were no longer interested in mating with the females.20
Snakes and lizards have highly developed senses of smell that can be utilized in
a training program; for example, an effective training method is to use a prey scent trail
to train a snake to move when needed, taking advantage of a natural predatory
behavior in the animal—seeking prey by scent—to accomplish a desired behavior
with reduced stress (Janis Gerrits, Washington, DC, personal communication, January
2012).
Reptiles are a diverse group of animals that require varied training approaches to
appeal to specific physiologic and behavioral tendencies or inclinations for each
taxon. When approaching training opportunities with such a vast number of different
species, the natural history, and communication channels of each should be studied
and incorporated into the training plan.

Reptile Cognition
It is a common misconception that ectotherms lack cognitive abilities. Research has
demonstrated that reptiles display behavioral complexity and have the ability to
learn.21–25 For example, behavioral complexity and play in a Komodo dragon (Vara-
nus komodoensis) at the Smithsonian’s National Zoo were documented by intro-
ducing a series of objects to the lizard. This study suggests significant cognitive
abilities of this large, long-lived reptile, which has been trained at many zoological
institutions to allow behavioral restraint for veterinary care. A related species, the
black throated monitor (Varanus albigularis), has also shown cognitive and problem
solving abilities, learning how to open a hinged door to gain access to food items.26
Operant conditioning has been increasingly used with reptiles in zoological settings
over the past 10 years22,23,25,27–29 to facilitate veterinary care and more complex
approaches reflecting reptile intelligence are being incorporated into training
programs. For example, 4 adult Aldabra tortoises (Geochelone gigantea) learned
to associate a clicker with food, to target, and then to hold still with their necks
extended to the target to allow venipuncture of the jugular vein.25 In another
example, a Nile crocodile (Crocodylus niloticus) was taught to associate a whistle
with food, then target and station on cue, which eventually allowed staff to obtain
a weight and blood draw without sedation or restraint.22 Studies in indigo snakes
(Drymarchon corais) have shown that their rate of response to operant conditioning
is similar to comparable studies of rats that had been trained to press levers or disc-
pecking pigeons.30
Previously mentioned examples of reptilian cognitive abilities and training suc-
cesses have focused on large animals that many veterinarians may never see in their
offices. However, there are examples of smaller reptile species displaying cognition.
Researchers at Duke University documented problem solving in the emerald anole
(Anolis evermanni), where the animal demonstrated the ability to problem solve by
removing a disc to gain access to a covered food item.31 The test subjects also
learned to discriminate between the target and a distracter disc placed in close prox-
imity to the target, displaying cognitive abilities and behavioral flexibility comparable to
many endothermic species. With documented case studies, new research emerging,
430 Hellmuth et al

and continued success in various reptile training programs in zoological settings, it is


clear that reptiles have significant cognitive abilities.

REPTILE TRAINING
Benefits of Operant Conditioning
Behavioral training has many purposes and benefits for animals including physical
exercise, mental stimulation, reducing stress, research, work and service functions,
increased safety, cooperative behavior, and more. But one of the most important
reasons for training animals is to better provide for the animals’ physical and mental
welfare.32 And contrary to the beliefs of some, there are no boundaries as to which
species can be trained.33
Veterinary care is an important part of a captive animal’s life, and it is in the best
interests of all involved to make the process as positive as possible. Stress can
have adverse impacts on reptiles and as such should be minimized when possible.
Studies on farm and laboratory animals show that handling for some veterinary proce-
dures can be stressful, but if the animals learn to associate desired consequences with
these interactions, the degree of fear responses they exhibit can be reduced.34 This is
certainly applicable to reptilian taxa, and should be considered when owning, housing,
and treating any captive specimen.
Training has proved to be beneficial in mammals, producing more accurate diag-
nostic analysis for biochemical data. In rhesus monkeys (Macaca mulatta), cortisol
levels were significantly higher when animals were trained versus restrained for
blood collection.35 Other research has shown reductions in stress hormones36,37
and stereotypic behavior38 as beneficial effects of training. Similar results have
been described in bongo (Tragelaphus euryceros) with significantly reduced cortisol
levels for crate-trained animals when restrained in the crate for 20 minutes,39,40 close
to baseline cortisol levels for resting cattle.41,42 The bongo trained for restraint had
lower creatine phosphokinase and glucose levels than animals immobilized by
dart or pole syringe.40 Livestock cared for by workers who build relationships (eg,
patting, stroking, moving slowly) versus ones who use aversive interactions (eg,
quick movements, shouting, hitting) showed reduced fear of humans.43,44 Lab-
housed stump-tailed macaques (Macaca actdoides) considered friendly by care-
takers received more attention and interactions, were less disturbed by procedures,
and were more likely to approach and accept food from caretakers.45 And in a zoo
study, reproduction in small exotic cats was more successful when keepers spent
time interacting with the animals.46 These studies are evidence that teaching animals
to cooperate in their own health care can make life less stressful for both the animal
and the trainer.32
Safety is a primary concern when working in close proximity to any animal. Both
animals and people are at risk due to fear-based behavior. Animals showing fear
responses can be dangerous animals.47 They are more likely to injure themselves or
their handlers than are animals that are not showing behaviors indicative of
fear.41,48,49 All vertebrates can learn to associate a fear response with certain
stimuli.50,51 Some animals learn to pair a fear response with the presence of the veter-
inarian.47 Operant conditioning can also be used to reduce fear responses and pair
positive reinforcers with the veterinarian and medical procedures. Training animals
to cooperate with handling procedures helps reduce stress and accidents,47 thus
improving safety for humans and animals alike (Box 1).
Even with potentially dangerous animals such as venomous snakes, there are
a variety of tools made specifically for working more safely with them, including hooks,
Operant Conditioning Techniques with Reptiles 431

Box 1
Case Study 1: Caiman Lizard (Dracaena guianensis), Schönbrunn Zoo, Vienna, Austria
The caiman lizard is a large, semi-aquatic lizard from the Amazon River basin can reach at least
412 mm SVL (snout-vent length). These carnivorous reptiles spend time both in trees and in
water, and hunt snails as their primary source of prey (Mesquita et al, 2006).
The Schönbrunn Zoo in Vienna, Austria received 2.2 caiman lizards from a breeding farm in
Peru in August 2008, when the animals were 8–12 months of age. Once the animals were stable
and eating consistently in an off exhibit area, they were moved to a large, 40 square meter
enclosure; designed with many plants, rock walls, a river with a pond, and a variety of climbing
structures. The lizards were fed their favorite food – apple snails – in two or three different
locations throughout the enclosure.

Left to right: Caiman lizard being desensitized to handling gloves, caiman lizard tar-
geted into box and on scale, caiman lizard targeting onto x-ray cassette for radiographs.
(Courtesy of Archiv Tiergarten Schönbrunn; Data from Mesquita DO, Colli GR, Costa GC,
et al. At The Water’s Edge: Ecology of Semiaquatic Teiids in Brazilian Amazon. J Herpetol
2006;40(2):221–9.)
432 Hellmuth et al

After a short time in their new exhibit, a variety of management problems arose. One female
lizard became quite dominant and aggressive towards the others, and was able to eat most of
the snails; and was also the likely culprit in a tail injury received by the other female. One of the
male lizards hid, probably in the rock wall, and wasn’t able to be located for several weeks.
To help mitigate these problems, a behavioral training program was implemented, with an
initial goal of being able to individually feed and check each animal regularly. A second goal
was to desensitize the lizards to handling, because after each time the animals were caught
up for any reason, they exhibited fear and stress behaviors for a long period afterwards.
Training began in a terrarium behind the scenes. Some individuals allowed keepers to
approach closely enough to offer snails with tweezers, and some required more intensive
training to get to this point. After spending some time pairing a clicker (as a bridging stimulus)
with a snail, a target pole was introduced, and the lizards soon learned to touch and follow the
target. Targeting was used to guide the lizards over a variety of different materials for desen-
sitization, such as cloth, metal, wood, and leather; and they learned to follow the target
through objects such as pipes and boxes, including into a transport crate. The desensitization
training allowed the staff to begin touching and handling the lizards with heavy leather gloves
without stressing the animals; and the targeting behavior also allowed keepers to train the
lizards to go into a crate voluntarily. The crating behavior was useful for a wide variety of other
management and veterinary behaviors, as the crate could easily be placed on a scale to obtain
weights, and over an x-ray film cassette for radiographs. The lizards were also able to be tar-
geted directly on to the film cassette for radiographs as well, which added flexibility in utilizing
this diagnostic tool.
The training program has been very successful in helping to better and more safely manage this
amazing species. The staff discovered that in addition to easier and less stressful handling, the
lizards are now more relaxed in the presence of the keepers and they show less aggression to
each other within the group.

tongs, shields, snake cans, and tubes.52 Utilizing the proper tools in combination with
operant conditioning techniques, it is possible to train many reptilian species regard-
less of their size or venomous nature (Box 2).

Utilizing Training in Veterinary Care


There are numerous behaviors that can be used to facilitate many aspects of veteri-
nary care, from diagnosing the problem to administering treatment. Reptiles respond
to operant conditioning, and training should be used to minimize stress and maximize
the ability to medically evaluate and treat these animals. This section will focus on
some of the more useful behaviors and their application to veterinary exams, and
will review specific examples (Appendix 1) of how training and desensitization enable
veterinary procedures with reduced stress.

Desensitization
“Desensitization is the process of getting an animal used to a new stimulus through
gradual exposure to it. The stimulus may be people, other animals, noises, lighting,
or anything the animal may perceive as new or frightening.”32 Desensitization can
be trained with both active and passive methods. Passive desensitization is called
habituation, where an animal gets used to new things on its own over time, without
active involvement from a trainer and without pairing the association with reinforce-
ment.32 With this technique the animal needs to be able to choose to go near or
interact with the new stimulus; it should not be forced into close proximity or it might
result in increased fear responses.53
Operant Conditioning Techniques with Reptiles 433

Box 2
Case Study 2: Nile crocodile (Crocodylus niloticus), Wildlife Conservation Society, Bronx Zoo,
Bronx NY
The Nile crocodile is a large predator native to Africa, which can grow to lengths of 6 meters
(Trutnau and Sommerland 2006). Likely because of their impressive size, Nile crocodiles are
one of the most commonly kept crocodilian species in captivity. However, their size and phys-
iology creates many challenges to maintaining them in captivity.
In response to these challenges, the Bronx Zoo utilized operant conditioning to facilitate exam-
ining and treating large crocodilians in captivity. A training program for an adult male Nile
crocodile was initiated in May 2008 soon after his arrival. First a whistle bridge was condi-
tioned; then a target behavior was trained. Initially mastering targeting in the water, the
animal’s potential was quickly seen and the keepers began opportunistically working him on
land.
To take this training further, a protocol for blood draw training was drafted. But before this
training could commence there were some safety concerns to be addressed. Entering the
exhibit with an eight-foot Nile crocodile is dangerous, and facility modifications were
completed to reduce the risks and safeguard the keeper and veterinary staff. The animal
was slowly habituated to human presence in the exhibit and then desensitized to touch on
his tail. With a combination of facility modifications for safety, desensitization to a variety of
people and stimuli, and step by step operant conditioning techniques, the crocodile was
able to be stationed on a scale and blood was successfully collected in March 2010.
The use of this training could have tremendous ramifications. By desensitizing this animal to
touch as well as habituating him to human presence, veterinarians can safely approach this
animal for physical exams, injury assessments and treatments. The collection of regular blood
samples could allow veterinary staff the ability to further study crocodilian disease and treat-
ment as well as document normal blood values for that animal and the species. In addition this
behavior could possible allow for injectable treatments on this animal if necessary.

Data from Trutnau L, Sommerland R. Crocodilians: Their Natural History and Captive
Husbandry. 1st edition. Frankfurt (Germany): Brahm AS; 2006.

Active desensitization, or counter conditioning, is a process where the new stimulus


is paired with or followed by reinforcement to create a positive association with that
stimulus.32 Counter conditioning gives the trainer more control over the process and
progress can frequently move at a more rapid pace than habituation. Both methods
of desensitization can be beneficial in the training of cooperative behaviors for veteri-
nary visits and examinations. The involvement of veterinarians in desensitization for
veterinary visits and medical behaviors is critical. They are needed stimuli that will be
present for procedures and should therefore be part of the training process. Other
training includes desensitizing the animal to the equipment that will be used, the phys-
ical contact that is required for the exam, the duration of the procedure, and the number
of people that need to be present.32
Taking the time to get animals used to and comfortable with the situations and equip-
ment they might encounter in a veterinary visit can go a long way in making a more
receptive and cooperative participant. The Denver Zoo routinely handles several
species of non-venomous snakes to desensitize them to veterinary exams (Patricia
Anderson, Denver, CO, personal communication, January 2012). At the Schönbrunn
Zoo in Austria, keepers desensitized their Caiman lizards (Dracaena sp) to leather
gloves and veterinary equipment to prepare them for veterinary visits (Dr Eveline Dungl,
Vienna, Austria, personal communication, January 2012) (Box 3). At the North Carolina
Zoo, keepers desensitized an American alligator to a sit under a nebulizer for pneu-
monia treatments (Chris Shupp, Asheboro, NC, personal communication, February
434 Hellmuth et al

Box 3
Case study 3: False water cobras (Hydrodynastes gigas), Smithsonian’s National Zoo,
Washington, DC
False water cobras are rear fanged, venomous colubrids that occur naturally in South America
(Greene, 1997). They are large semi-aquatic snakes, feeding mostly on frogs and fishes (Bels,
1987; Strüssmann & Sazima, 1993). Their biology makes them great exhibit animals, utilizing
aquatic, terrestrial, and arboreal features in the exhibit at the Smithsonian’s National Zoo.
Three juvenile false water cobras are exhibited together in the Reptile Discovery Center. When
multiple snakes are housed together, feeding the animals in a manner that avoids conflict,
aggression, and possible ophiophagia (eating of the other snakes) is of top concern and usually
results in the animals being separated during feeding. Typically, venomous snakes are hooked
off-exhibit into a secure holding container (referred to as canning) for routine exhibit mainte-
nance and feedings. False water cobras are known to be very active, vigorous feeders which can
be a challenge, but in this circumstance, proved to be a wonderful training opportunity. To
date, each individual animal has been successfully trained to follow a scented target pole
into an off-exhibit holding can for each feeding session. By scenting a target stick, animals
are enticed to follow the target stick and willingly enter the can. The animal is rewarded for
this behavior with mice left in the bottom of the can.
This has proven to be an effective tactic used while performing routine husbandry practices,
and many future uses as well. It is now a very easy task to weigh and manipulate the animals
into any number of containers for safe handling, allowing for veterinary assessment and
possible treatments. Additionally, this training likely reduces the stress for animals and keepers
by minimizing hooking efforts, as well as decreasing the time it takes to separate and move
animals.

Data from Refs.65–67

2012); and at the Fort Worth Zoo, a Komodo dragon has been desensitized by the
keeper staff and is trained to allow a mask to be placed on its head for anesthesia during
veterinary exams (Diane Barber, Fort Worth, TX, personal communication, February
2012).
Animals that are regularly handled for routine procedures are likely to experience
less stress when captured for an uncommon procedure.54 As one trainer put it, “We
teach the animals to help us take care of them . we teach the animals that going
to the vet is a game and we play that game every single day, whether a vet is there
or not. And those ‘games’ include numerous veterinary or cooperative behaviors. To
the animal, it’s just part of the training session.”55

Tactile Desensitization
An important behavior to teach animals for a veterinary examination is to accept tactile
stimulation.56 While not every species or individual is amenable to this technique,
animals that have been taught to accept being touched will be easier to manage.
And, although some animals may seem to solicit petting or tactile interactions, this
does not automatically mean they will do so for medical procedures. Desensitization
is a critical component to establishing reliable tactile interactions and is helpful for
husbandry procedures.32 Tactile desensitization training should begin with parts of
the body where the animal is most receptive to touch, and the animal should never
be surprised by the touch.57 Animals should be made aware that a touch is going to
occur, either through a verbal signal or other sensory cue. This strategy can help
reduce potential aggressive behavior from a surprised animal and help prevent
damaging the trust between the trainer and animal.56
Operant Conditioning Techniques with Reptiles 435

At the Smithsonian’s National Zoo, daily habituation and tactile desensitization has
become a key component in the medical care of an adult male Komodo dragon. As
part of this animal’s management, cleaning and exhibit maintenance are done in the
morning, and feeding in the afternoon. Every morning, when the animal’s body
temperature is lower and it is less active, the keeper completes the needed exhibit
work and then engages the animal with tactile interaction. Over time, the lizard has
become habituated to this routine, and the veterinary team is able to enter the animal’s
enclosure and obtain radiographs without heavy restraint or sedation (Janis Gerrits,
Washington, DC, personal communication, January 2012).

Targeting/Stationing
Basic behaviors such as targeting and stationing are excellent ways to position and
manipulate an animal in order to better assess health concerns. A target is an object
that an animal is taught to touch, follow, or go to. It can be a ball on the end of a stick,
a hand, a straw, spoon, or any object that the animal can perceive and is safe to use.
Once an animal understands the target behavior concept, targeting can be used as
a tool in training many other behaviors. It can be part of an active desensitization
program, where an animal follows a target to, and even on or through, novel items
(Dr Eveline Dungl, Vienna, Austria, personal communication, January 2012). It can
be used to teach an animal to go onto a scale, into a crate, and countless other behav-
iors. For example, the Colchester Zoo used the targeting behavior to move their croc-
odiles and Komodo dragons for examination, to obtain weights, blood draws, ultra
sounds, nail trims, and to apply topical medication (Jez Smith, Essex, United
Kingdom, personal communication, January 2012). These behaviors are sometimes
initiated with baiting or luring—where the animal is shown food or food is put on/in
the desired item (ie, crate or scale) to entice the animal to approach. Baiting, while
a useful training tool, can be problematic if the animal needs to be fasted for medical
reasons but requires food in order to perform a task.56 Targeting is a much more effec-
tive tool in these instances.
Stationing is an offshoot of the targeting behavior; it refers to training an animal to go
to a specific item or location, and tells the animal where it is expected to be for
a behavior or during a training session.32 When training a reptile for veterinary care,
the station can be a familiar item that carries reinforcement value in an unfamiliar envi-
ronment. For example, if an animal is trained to station on a piece of Astroturf, this can
easily be brought to the veterinarian’s office and put on a scale or exam table for
stationing during the exam.
Both stationing and targeting are foundation behaviors that are at the core of a good
training program. If they are trained to fluency, they offer the animal the opportunity to
present a behavior that has a strong history of positive reinforcement in a veterinary
setting. This can potentially lead to a more relaxed and cooperative patient in an unfa-
miliar environment.

Box/Squeeze/Tube
Training an animal to enter a mobile shift or squeeze box can reduce stress for trans-
portation and can be useful for basic husbandry. This can be a permanent or tempo-
rary attachment to the animal’s enclosure and should be dark, warm, or in some way
attractive to the reptile. Animals can be fed in the shift box, so that the reptile has
a positive association with the shift. At the Buffalo Zoo, black tree monitors (Varanus
beccarii) have been trained to station in a plastic container for weighing (Penny Felski
and Illa Caira, Buffalo, NY, personal communication, February 2012).
436 Hellmuth et al

The shift box can be a clear, acrylic squeeze cage so that the patient can be visually
inspected by the veterinarian, and so that the animal can be restrained into a smaller
space to receive injections, facilitate anesthesia, or accomplish blood draws. Several
institutions have animals trained to enter clear containers for veterinary exams,
including poison dart frogs (Dendrobates sp) at Disney’s Animal Kingdom (Mindy
Sommer, Lake Buena Vista, FL, personal communication, January 2012), green
mamba (Dendroaspis angusticeps) at the Brookfield Zoo (Tim Sullivan, Brookfield,
IL, personal communication, January 2012), and Komodo dragons at the Toronto
Zoo (Nicole Presley, Toronto, Canada, personal communication, February 2012),
and Singapore Zoo (Sarah Chin, Singapore, personal communication, February 2012).
Another tool is a snake immobilization tube that, when combined with operant
conditioning, can be a highly effective method for safely handling and examining
venomous species. Operant conditioning can be used to train the snake to enter
the tube voluntarily rather than with force. One method utilized at the Riverbanks
Zoo was to use the targeting behavior to train a king cobra to enter a tube. This,
however, proved more difficult than anticipated so keepers had to initially bait, or
used food to entice the animal into the tube.28 Baiting allowed the animal handlers
to desensitize and eventually target train the snake into the tube.28

CHALLENGES IN TRAINING REPTILES

Although training is a useful tool for facilitating veterinary care, there are many chal-
lenges that must be addressed when training reptile species. It is important to
remember the animal’s health and welfare is top priority, and training should not
commence if it compromises the animal’s health.

Overfeeding
The food requirements of reptiles vary depending on the specimens’ size, age,
temperature, activity,58 and reproductive status.59 As ectotherms, reptiles are charac-
terized by low metabolic rates and high conversion efficiencies.60 Overfeeding is
a commonly seen problem with amateur herpetologists.61,62 Obesity can increase
the likelihood of liver disease, cardiac disease, arthritis, and renal disease.58 When
designing a training program it is imperative to keep the animal’s diet consistent
and appropriate for the species and individual.

Frequency of Feeding
The time and frequency of feeding reptiles is of significant importance when training.
Some species will readily eat any time, while others are strictly nocturnal or diurnal
feeders.63 Additionally, many species will fast for weeks or months in the wild as an
adaptation to the natural environment or reproductive status and this can persist in
captivity.63 The frequency in which animals are trained and fed will directly affect
the success of a training program. Most mammals eat several times a day, making
the potential training regimen much more intensive than that of a reptile that can
consume as little as 1 meal a month in captivity. In order to maximize training sessions
with these animals, it is imperative to use every feeding session as an opportunity to
train the animal. Caregivers can increase the frequency of training and still maintain the
animal’s caloric intake by offering smaller food items that, cumulatively, are the equiv-
alent to one large meal. Feeding several small items or portions instead of one large
meal can increase training approximations during each individual session.29 Each
species’ natural feeding behavior should be taken into consideration when a dietary
change is made for training purposes. For example, grazers such as tortoises can
Operant Conditioning Techniques with Reptiles 437

easily have their diet split up and offered to them throughout the day, but this strategy
may not be as feasible with all reptilians.

Food Delivery
Understanding how reptiles perceive the world is important when feeding a captive
specimen. Reptiles use several senses simultaneously when feeding; in particular
olfactory, visual, and thermal cues. When approaching an enclosure with food, the
olfactory cue has likely been delivered and the next cue is the visual presentation
of food. Reptiles have varying degrees of vision, snakes for the most part have relin-
quished an emphasis on visual cues19 where lizards are often utilizing vision for prey
and mate selection.64
A challenging aspect of training reptiles is delivering the food reinforcer safely and in
a timely manner, especially when working with venomous species and/or animals
known for aggressive behavior. This can then be exacerbated when multiple animals
are in an enclosure together. Hand delivery of food poses risks. Hand delivery requires
the trainer’s hand to get within close proximity of the reptiles’ mouth. If tossing the food,
there is a chance the animal may miss the food item and/or see the movement of the
trainer’s hand and perceive that quick motion as the food. Both of these examples
can cause injury or adversely affect training outcomes. Many tools are available to effec-
tively deliver food to animals when training including tongs, feeding sticks and forceps.
If an animal is hesitant to approach the caregiver, proximity training can be an effec-
tive method of slowly desensitizing the animal to a person’s presence during feeding.
This training, combined with the different lengths of tongs available, can ease the
animal into the new feeding regime.
When utilizing feeding tools the delivery is often slower, providing the animal with
a number of cues or signals that food is coming, making reinforcing the desired
behavior challenging. The olfactory cue, in combination with a slow delivery of food,
can elicit an aggressive feeding response that may inadvertently be reinforced. This
type of feeding response can be minimized by training the animal to sit at a station
where feeding will occur.
Tools, especially tongs, are often used for cleaning, feeding and manipulating the
animal or cage furniture. When a tool is used repeatedly to feed an animal, the animal
may form an association between it and the food. When used for other purposes, the
tongs will likely elicit a feeding response even when not being used for feeding. Addi-
tionally an animal can sustain an injury during tong feeding if it is overly motivated to
feed. Animals that are new to tong feeding tend to bite the tongs and abrade in and
around the mouth. This can be avoided by using padded tongs, and reinforcing and
shaping a calm feeding behavior.
A feeding stick is another option for delivering food reinforcers. A dowel rod or
other similar item can easily be fashioned into a feeding stick by whittling one end
into a dull point. This point can be used to skewer food onto the end of the rod,
without posing a danger to the animal. Another tool option is forceps, which are
used much like tongs and come in a variety of lengths. These are appropriate for
aquatic species and species that eat small prey. They will allow delivery of the
food while maintaining a safe and comfortable distance, without overpowering the
food with a large delivery tool. Forceps might also minimize the feed response to
a multipurpose tool like tongs.

Environmental Conditions
The environmental conditions that are ideal for keeping reptiles can prove to be yet
another challenge for training. Reptile enclosures are usually small, are kept at higher
438 Hellmuth et al

temperatures, and are uniquely designed to the species being exhibited. For example,
an enclosure might require a significant amount of perching for a particular species or
a large pool of water for a semi-aquatic species. When attempting to train a reptile,
especially a small lizard or snake, the door must often remain open during the session.
When working with quick moving species, minimizing or eliminating animal escapes
needs to be a priority. To avoid escapes from enclosures, it is best to move the animal
to a more appropriate training space, or when this is not possible, training the animal
to station away from the door can increase safety and reduce the risk of an escape.
Reptiles may be housed individually, in pairs, or in social groups. Housing animals
together may cause dominance hierarchies amongst the animals, and more dominant
animals to over-eat while submissive animals receive less food. Dominant animals will
generally be more easily trained. Forming a relationship with the more submissive
animal can be difficult, especially with the dominant animal(s) present. Removing
a reptile from the enclosure can help focus on training goals with the other animal.
At the Smithsonian’s National Zoo a keeper trained a very active and food motivated
Mertens’ water monitor (Varanus mertensi) to follow a target into a holding container in
order to isolate and train the animal’s exhibit mate (Janis Gerrits, Washington, DC,
personal communication, January 2012).
Paradigm Shift
While the use of operant conditioning training to facilitate management and veterinary
care has gained more widespread acceptance in recent years, its application with
reptiles and amphibians has lagged behind that of their mammal and avian counter-
parts. This could be due to the ease with which many reptiles can be involuntarily picked
up or restrained for examinations, or it could be related to the lack of reptile and
amphibian training models for caregivers to learn from. For those who work with or
own mammals or birds, they can look to an abundance of examples of training; from
dog training for obedience and agility to an array of animal shows at zoos and aquariums
with a wide variety of taxa. Even when reptiles are involved in these types of shows and
demonstrations, they are generally carried or held, and rarely are shown being trained to
exhibit active or natural behaviors during these programs. A paradigm shift is needed,
with keepers, owners, and veterinarians learning about and embracing the benefits of
operant conditioning as a critical component in the care of reptiles and amphibians.
Even once this paradigm shift occurs, a challenge still remains. Operant conditioning
is a skill set that must be learned; reptile owners and veterinarians need to make an
effort to learn this useful technology to benefit their animals. While there are many
wonderful training resources available, there are none dedicated to the specific chal-
lenges of working with reptiles and amphibians. Fortunately, training is training, and
the art and science of animal training is transferable to any species, any animal.53

SUMMARY

Reptiles are capable of responding to operant conditioning and should have training
programs incorporated into their captive husbandry. Of the many benefits training
affords, the most important is its use in diagnosing and treating an ill animal. Veterinary
clinicians should inform their clientele about the benefits operant conditioning can
provide for the reptiles in their care.

ACKNOWLEDGMENTS

We would like to thank everyone who responded to our surveys and shared their
training experiences for use in this article: Patricia Anderson, Denver Zoo; Diane
Operant Conditioning Techniques with Reptiles 439

Barber, Fort Worth Zoo; Jason Brock, Zoo Atlanta; Sarah Chin, Singapore Zoo; Dr
Eveline Dungl, Schönbrunn Zoo; Penny Felski and Illa Caira, Buffalo Zoo; Janis Gerrits,
Smithsonian’s National Zoological Park; Justin Graves, Smithsonian’s National
Zoological Park; Raelene Hobbs, Melbourne Zoo; Jack M. Jewell, Mandalay Bay
Aquarium; April Martin, National Aquarium in Baltimore; Darren Minier, University of
California at Davis; Shannon Osterholm, Blank Park Zoo; Nicole Presley, Toronto
Zoo; Nelly Rivera, Theater of the Sea; Chris Shupp, North Carolina Zoo; Jez Smith,
Colchester Zoo; Mindy Sommer, Disney’s Animal Kingdom; Jake Steventon,
Tennessee Aquarium; Tim Sullivan, Chicago Zoological Society; and Kevin Torre-
grosa, St Augustine Alligator Farm.

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APPENDIX 1: EXAMPLES OF TRAINED BEHAVIORS FOR FACILITATING VETERINARY


PROCEDURES IN REPTILE SPECIES FROM ZOOLOGICAL INSTITUTIONS WORLDWIDE

Institution Species Behaviors


Blank Park Zoo, IA Aldabra tortoise, Target (weights, moves),
Geochelone gigantea Mouth open (oral exam)
Desensitization (blood
draws, diagnostic imaging,
eye drops, eye pressure
test, weights, foot exam)
Buffalo Zoo, NY Black tree monitor, Varanus Shift/Plastic container
beccarii (weights, visual exam,
diagnostic imaging)
Chicago Zoological Society- American alligator, Alligator Eye drops
Brookfield Zoo, IL mississippiensis
Green mamba, Dendroaspis Shift container (anesthesia,
angusticeps exams)
Colchester Zoo, United Komodo dragon, Varanus Station/Desensitization
Kingdom komodoensis (diagnostic imaging, blood
draws, nail trims, topical
medications, weights)
Crocodiles (various sp) Target (exam)
Disney’s Animal Kingdom, FL Dart frogs, Dendrobates sp Station (exam, weights)
Denver Zoo, CO American alligator, Alligator Station (reduce aggression)
mississippiensis
Various species Station/Desensitization (exam)
Fort Worth Zoo, TX Komodo dragon, Varanus Desensitization (anesthesia)
komodoensis
Water/yellow tree monitor, Target/Desensitization (exam),
Varanus sp Crate (exam, moves)
Target (exam), Station (exam,
Indian gharial, Gavialis oral medications)
gangeticus
Mandalay Bay, NV Komodo dragon, Varanus Target (exam, moves),
komodoensis Desensitization (nail trims),
Crate (diagnostic imaging,
exam, blood draws)
Target (exam, moves), Crate
Crocodiles/sea turtles (diagnostic imaging, exam,
(various sp) blood draws)
Melbourne Zoo, Australia Aldabra tortoise, Target (weights),
Geochelone gigantea Desensitization (exam,
blood draws, topical
medications, diagnostic
imaging, mouth
inspection)
Operant Conditioning Techniques with Reptiles 443

Riverbanks Zoo, SC King cobra, Ophiophagus Shift/Tube (exam)


hannah
Schönbrunn Zoo, Austria Morlett’s crocodile, Target (moves)
Crocodylus moreletii
Giant tortoise (various sp) Target (moves, weights),
Desensitization (exam)
Caiman lizard, Dracaena Crate (weight, diagnostic
guianensis imaging), Desensitization
(handling with gloves)
Sedgwick County Zoo, KS Aldabra tortoise, Target (weights), Station/
Geochelone gigantea Desensitization (blood
draws)
Singapore Zoo, Singapore Komodo dragon, Varanus Target (exam, moves),
komodoensis Desensitization (exam,
diagnostic imaging)
Smithsonian’s National Poison dart frogs, Target (move to increase UVB
Zoo, DC Dendrobates sp intake)
Indian gharial, Gavialis Crate (moves)
gangeticus
Aldabra tortoise, Target (weights), Station
Geochelone gigantea (cooperative feeding)
Komodo dragon, Varanus Desensitization (exam,
komodoensis diagnostic imaging)
False water cobra, Target (shift off exhibit)
Hydrodynastes gigas
Theater of the Sea, FL American alligator, Alligator Target (moves, exam), Lift
mississippiensis feet (exam, topical
medications), Station
(weights)
Toronto Zoo, Canada Komodo dragon, Varanus Shift/Crate (exam, nail trims,
komodoensiss diagnostic imaging)
Dwarf crocodile, Shift (exam)
Osteolaemus tetraspis
Nile monitor, Varanus Shift (exam)
niloticus
Chinese softshell turtle, Target (exam)
Pelodiscus sinensis
American alligator, Alligator Target (move, exam)
mississippiensis
Nile softshell turtle, Trionyx Target (exam, weights),
triunguis Desensitization (shell
scrubs, topical
medications, exam, crate)
UC Davis, CA Snakes, tortoises, lizards Desensitization (restraint,
(various sp) exam, injections,
diagnostic imaging,
anesthesia)
Wildlife Conservation Nile crocodile, Crocodylus Target (exam), Station (exam,
Society-Bronx Zoo, NY niloticus weights), Desensitization
(exam, blood draws, zip-tie
on snout)
Zoo Atlanta, GA Aldabra tortoise, Target (weight, exam)
Geochelone gigantea
Komodo dragon, Varanus Station (on wire mesh for
komodoensis nail trims)

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